Abstract

Each year almost 300,000 individuals worldwide are diagnosed with oral cancer, more than 90% of these being oral carcinoma [N. Engl. J. Med. 328, 184 1993]. Surgical resection is the standard of care, but accurate delineation of the tumor boundaries is challenging, resulting in either under-resection with risk of local recurrence or over-resection with increased functional loss and negative impact on quality of life. This study evaluates, in two pre-clinical in vivo tumor models, the potential of fluorescence-guided resection using molecular beacons activated by metalloproteinases, which are frequently upregulated in human oral cancer. In both models there was rapid (<15 min) beacon activation upon local application, allowing clear fluoresecence imaging in vivo and confirmed by ex vivo fluorescence microscopy and HPLC, with minimal activation in normal oral tissues. Although the tissue penetration was limited using topical application, these findings support further development of this approach towards translation to first-in-human trials.

© 2016 Optical Society of America

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2016 (1)

M. J. Whitley, D. M. Cardona, A. L. Lazarides, I. Spasojevic, J. M. Ferrer, J. Cahill, C.-L. Lee, M. Snuderl, D. G. Blazer, E. S. Hwang, R. A. Greenup, P. J. Mosca, J. K. Mito, K. C. Cuneo, N. A. Larrier, E. K. O’Reilly, R. F. Riedel, W. C. Eward, D. B. Strasfeld, D. Fukumura, R. K. Jain, W. D. Lee, L. G. Griffith, M. G. Bawendi, D. G. Kirsch, and B. E. Brigman, “A mouse-human phase 1 co-clinical trial of a protease-activated fluorescent probe for imaging cancer,” Sci. Transl. Med. 8(320), 320ra4 (2016).
[Crossref] [PubMed]

2015 (1)

T. W. Liu, J. Chen, L. Burgess, B. C. Wilson, G. Zheng, L. Zhan, W. K. Liu, and B. Y. Ha, “Activation Kinetics of Zipper Molecular Beacons,” J. Phys. Chem. B 119(1), 44–53 (2015).
[Crossref] [PubMed]

2014 (1)

A. Scerrati, G. M. Della Pepa, G. Conforti, G. Sabatino, A. Puca, A. Albanese, G. Maira, E. Marchese, and G. Esposito, “Indocyanine green video-angiography in neurosurgery: A glance beyond vascular applications,” Clin. Neurol. Neurosurg. 124, 106–113 (2014).
[Crossref] [PubMed]

2013 (1)

Q. T. Nguyen and R. Y. Tsien, “Fluorescence-guided surgery with live molecular navigation - a new cutting edge,” Nat. Rev. Cancer 13(9), 653–662 (2013).
[Crossref] [PubMed]

2012 (3)

M. Junaid, M. M. Choudhary, Z. A. Sobani, G. Murtaza, S. Qadeer, N. S. Ali, M. J. Khan, and A. Suhail, “A comparative analysis of toluidine blue with frozen section in oral squamous cell carcinoma,” World J. Surg. Oncol. 10(1), 57 (2012).
[Crossref] [PubMed]

M. Rana, A. Zapf, M. Kuehle, N. C. Gellrich, and A. M. Eckardt, “Clinical evaluation of an autofluorescence diagnostic device for oral cancer detection: a prospective randomized diagnostic study,” Eur. J. Cancer Prev. 21(5), 460–466 (2012).
[Crossref] [PubMed]

C. S. Farah, L. McIntosh, A. Georgiou, and M. J. McCullough, “Efficacy of tissue autofluorescence imaging (VELScope) in the visualization of oral mucosal lesions,” Head Neck 34(6), 856–862 (2012).
[Crossref] [PubMed]

2011 (4)

M. Scheer, J. Neugebauer, A. Derman, J. Fuss, U. Drebber, and J. E. Zoeller, “Autofluorescence imaging of potentially malignant mucosa lesions,” Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod. 111(5), 568–577 (2011).
[Crossref] [PubMed]

W. Jerjes, T. Upile, Z. Hamdoon, C. A. Mosse, S. Akram, and C. Hopper, “Photodynamic therapy outcome for oral dysplasia,” Lasers Surg. Med. 43(3), 192–199 (2011).
[Crossref] [PubMed]

T. W. B. Liu, J. Chen, and G. Zheng, “Peptide-based molecular beacons for cancer imaging and therapy,” Amino Acids 41(5), 1123–1134 (2011).
[Crossref] [PubMed]

T. W. Liu, M. K. Akens, J. Chen, L. Wise-Milestone, B. C. Wilson, and G. Zheng, “Imaging of specific activation of photodynamic molecular beacons in breast cancer vertebral metastases,” Bioconjug. Chem. 22(6), 1021–1030 (2011).
[Crossref] [PubMed]

2010 (1)

J. C. Brenner, M. P. Graham, B. Kumar, L. M. Saunders, R. Kupfer, R. H. Lyons, C. R. Bradford, and T. E. Carey, “Genotyping of 73 UM-SCC head and neck squamous cell carcinoma cell lines,” Head Neck 32(4), 417–426 (2010).
[PubMed]

2009 (5)

S. Nagini, P. V. Letchoumy, A. Thangavelu, and C.R. Ramachandran, “Of humans and hamsters: A comparative evaluation of carcinogen activation, DNA damage, cell proliferation, apoptosis, invasion, and angiogenesis in oral cancer patients and hamster buccal pouch carcinomas,” Oral Oncol. 45(6), e31–e37 (2009).
[Crossref] [PubMed]

C.-Y. Wang, T. Tsai, C.-P. Chiang, H.-M. Chen, and C.-T. Chen, “Improved diagnosis of oral premalignant lesions in submucous fibrosis patients with 5-aminolevulinic acid induced PpIX fluorescence,” J. Biomed. Opt. 14(4), 044026 (2009).
[Crossref] [PubMed]

J. de Leeuw, N. van der Beek, W. D. Neugebauer, P. Bjerring, and H. A. Neumann, “Fluorescence detection and diagnosis of non-melanoma skin cancer at an early stage,” Lasers Surg. Med. 41(2), 96–103 (2009).
[Crossref] [PubMed]

V. Jayaprakash, M. Sullivan, M. Merzianu, N. R. Rigual, T. R. Loree, S. R. Popat, K. B. Moysich, S. Ramananda, T. Johnson, J. R. Marshall, A. D. Hutson, T. S. Mang, B. C. Wilson, S. R. Gill, J. Frustino, A. Bogaards, and M. E. Reid, “Autofluorescence-guided surveillance for oral cancer,” Cancer Prev. Res. (Phila.) 2(11), 966–974 (2009).
[Crossref] [PubMed]

C. F. Poh, C. E. MacAulay, L. Zhang, and M. P. Rosin, “Tracing the “at-risk” oral mucosa field with autofluorescence: Steps toward clinical impact,” Cancer Prev. Res. (Phila.) 2(5), 401–404 (2009).
[Crossref] [PubMed]

2008 (4)

X. Wang, L. Yang, Z. G. Chen, and D. M. Shin, “Application of nanotechnology in cancer therapy and imaging,” CA Cancer J. Clin. 58(2), 97–110 (2008).
[Crossref] [PubMed]

A. M. Wu and T. Olafsen, “Antibodies for molecular imaging of cancer,” Cancer J. 14(3), 191–197 (2008).
[Crossref] [PubMed]

R. L. Scherer, J. O. McIntyre, and L. M. Matrisian, “Imaging matrix metalloproteinases in cancer,” Cancer Metastasis Rev. 27(4), 679–690 (2008).
[Crossref] [PubMed]

E. H. Moriyama, A. Kim, A. Bogaards, L. Lilge, and B. C. Wilson, “A Ratiometric Fluorescence Imaging System for Surgical Guidance,” Adv. Opt. Technol. 2008, 1–10 (2008).
[Crossref]

2007 (2)

G. Zheng, J. Chen, K. Stefflova, M. Jarvi, H. Li, and B. C. Wilson, “Photodynamic molecular beacon as an activatable photosensitizer based on protease-controlled singlet oxygen quenching and activation,” Proc. Natl. Acad. Sci. U.S.A. 104(21), 8989–8994 (2007).
[Crossref] [PubMed]

C. F. Poh, S. P. Ng, P. M. Williams, L. Zhang, D. M. Laronde, P. Lane, C. Macaulay, and M. P. Rosin, “Direct fluorescence visualization of clinically occult high-risk oral premalignant disease using a simple hand-held device,” Head Neck 29(1), 71–76 (2007).
[Crossref] [PubMed]

2006 (2)

W. Stummer, U. Pichlmeier, T. Meinel, O. D. Wiestler, F. Zanella, H.-J. Reulen, and ALA-Glioma Study Group, “Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: a randomised controlled multicentre phase III trial,” Lancet Oncol. 7(5), 392–401 (2006).
[Crossref] [PubMed]

T. Mang, J. Kost, M. Sullivan, and B. C. Wilson, “Autofluorescence and Photofrin-induced fluorescence imaging and spectroscopy in an animal model of oral cancer,” Photodiagn. Photodyn. Ther. 3(3), 168–176 (2006).
[Crossref] [PubMed]

2005 (1)

D. C. G. De Veld, M. J. H. Witjes, H. J. C. M. Sterenborg, and J. L. N. Roodenburg, “The status of in vivo autofluorescence spectroscopy and imaging for oral oncology,” Oral Oncol. 41(2), 117–131 (2005).
[Crossref] [PubMed]

2004 (3)

E. Svistun, R. Alizadeh-Naderi, A. El-Naggar, R. Jacob, A. Gillenwater, and R. Richards-Kortum, “Vision enhancement system for detection of oral cavity neoplasia based on auto fluorescence,” Head Neck 26(3), 205–215 (2004).
[Crossref] [PubMed]

W. Tan, K. Wang, and T. J. Drake, “Molecular beacons,” Curr. Opin. Chem. Biol. 8(5), 547–553 (2004).
[Crossref] [PubMed]

P. J. Santangelo, B. Nix, A. Tsourkas, and G. Bao, “Dual FRET molecular beacons for mRNA detection in living cells,” Nucleic Acids Res. 32(6), e57 (2004).
[Crossref] [PubMed]

2002 (1)

C. S. Betz, H. Stepp, P. Janda, S. Arbogast, G. Grevers, R. Baumgartner, and A. Leunig, “A comparative study of normal inspection, autofluorescence and 5-ALA-induced PPIX fluorescence for oral cancer diagnosis,” Int. J. Cancer 97(2), 245–252 (2002).
[Crossref] [PubMed]

2000 (3)

J. J. Li, R. Geyer, and W. Tan, “Using molecular beacons as a sensitive fluorescence assay for enzymatic cleavage of single-stranded DNA,” Nucleic Acids Res. 28(11), E52 (2000).
[Crossref] [PubMed]

A. Leunig, C. S. Betz, M. Mehlmann, H. Stepp, S. Arbogast, G. Grevers, and R. Baumgartner, “Detection of squamous cell carcinoma of the oral cavity by imaging 5-aminolevulinic acid-induced protoporphyrin IX fluorescence,” Laryngoscope 110(1), 78–83 (2000).
[Crossref] [PubMed]

W. Stummer, A. Novotny, H. Stepp, C. Goetz, K. Bise, and H. J. Reulen, “Fluorescence-guided resection of glioblastoma multiforme by using 5-aminolevulinic acid-induced porphyrins: a prospective study in 52 consecutive patients,” J. Neurosurg. 93(6), 1003–1013 (2000).
[Crossref] [PubMed]

1999 (1)

R. Weissleder, C.-H. Tung, U. Mahmood, and A. Bogdanov., “In vivo imaging of tumors with protease-activated near-infrared fluorescent probes,” Nat. Biotechnol. 17(4), 375–378 (1999).
[Crossref] [PubMed]

1998 (1)

S. Lam, T. Kennedy, M. Unger, Y. E. Miller, D. Gelmont, V. Rusch, B. Gipe, D. Howard, J. C. LeRiche, A. Coldman, and A. F. Gazdar, “Localization of bronchial intraepithelial neoplastic lesions by fluorescence bronchoscopy,” Chest 113(3), 696–702 (1998).
[Crossref] [PubMed]

1996 (3)

P. M. Speight, P. M. Farthing, and J. E. Bouquot, “The pathology of oral cancer and precancer,” Curr. Diagn. Pathol. 3(3), 165–176 (1996).
[Crossref]

K. F. M. Fan, C. Hopper, P. M. Speight, G. Buonaccorsi, A. J. MacRobert, and S. G. Bown, “Photodynamic therapy using 5-aminolevulinic acid for premalignant and malignant lesions of the oral cavity,” Cancer 78(7), 1374–1383 (1996).
[Crossref] [PubMed]

S. Tyagi and F. R. Kramer, “Molecular beacons: probes that fluoresce upon hybridization,” Nat. Biotechnol. 14(3), 303–308 (1996).
[Crossref] [PubMed]

1995 (1)

J. Kusukawa, Y. Sasaguri, M. Morimatsu, and T. Kameyama, “Expression of matrix metalloproteinase-3 in Stage I and II squamous cell carcinoma of the oral cavity,” J. Oral Maxillofac. Surg. 53(5), 530–534 (1995).
[Crossref] [PubMed]

1994 (1)

N. Ramanujam, M. F. Mitchell, A. Mahadevan, S. Warren, S. Thomsen, E. Silva, and R. Richards-Kortum, “In vivo diagnosis of cervical intraepithelial neoplasia using 337-nm-excited laser-induced fluorescence,” Proc. Natl. Acad. Sci. U.S.A. 91(21), 10193–10197 (1994).
[Crossref] [PubMed]

1993 (4)

D. Muller, C. Wolf, J. Abecassis, R. Millon, A. Engelmann, G. Bronner, N. Rouyer, M. C. Rio, M. Eber, G. Methlin, and P. Basset, “Increased stromelysin 3 gene expression is associated with increased local invasiveness in head and neck squamous cell carcinomas,” Cancer Res. 53(1), 165–169 (1993).
[PubMed]

W. E. Grant, C. Hopper, A. J. MacRobert, P. M. Speight, and S. G. Bown, “Photodynamic therapy of oral cancer: photosensitisation with systemic aminolaevulinic acid,” Lancet 342(8864), 147–148 (1993).
[Crossref] [PubMed]

I. B. Gimenez-Conti and T. J. Slaga, “The hamster cheek pouch carcinogenesis model,” J. Cell. Biochem. Suppl. 53(S17F), 83–90 (1993).
[Crossref] [PubMed]

J. Kusukawa, Y. Sasaguri, I. Shima, T. Kameyama, and M. Morimatsu, “Expression of matrix metalloproteinase-2 related to lymph node metastasis of oral squamous cell carcinoma. A clinicopathologic study,” Am. J. Clin. Pathol. 99(1), 18–23 (1993).
[PubMed]

1992 (2)

C. G. Knight, F. Willenbrock, and G. Murphy, “A novel coumarin-labelled peptide for sensitive continuous assays of the matrix metalloproteinases,” FEBS Lett. 296(3), 263–266 (1992).
[Crossref] [PubMed]

S. T. Gray, R. J. Wilkins, and K. Yun, “Interstitial collagenase gene expression in oral squamous cell carcinoma,” Am. J. Pathol. 141(2), 301–306 (1992).
[PubMed]

1991 (1)

M. Polette, C. Clavel, D. Muller, J. Abecassis, I. Binninger, and P. Birembaut, “Detection of mRNAs encoding collagenase I and stromelysin 2 in carcinomas of the head and neck by in situ hybridization,” Invasion Metastasis 11(2), 76–83 (1991).
[PubMed]

1988 (1)

W. J. Blot, J. K. McLaughlin, D. M. Winn, D. F. Austin, R. S. Greenberg, S. Preston-Martin, L. Bernstein, J. B. Schoenberg, A. Stemhagen, and J. F. Fraumeni., “Smoking and drinking in relation to oral and pharyngeal cancer,” Cancer Res. 48(11), 3282–3287 (1988).
[PubMed]

1980 (1)

G. Shklar, J. Schwartz, D. Grau, D. P. Trickler, and K. D. Wallace, “Inhibition of hamster buccal pouch carcinogenesis by 13-cis-retinoic acid,” Oral Surg. Oral Med. Oral Pathol. 50(1), 45–52 (1980).
[Crossref] [PubMed]

1953 (1)

D. P. Slaughter, H. W. Southwick, and W. Smejkal, “Field cancerization in oral stratified squamous epithelium; clinical implications of multicentric origin,” Cancer 6(5), 963–968 (1953).
[Crossref] [PubMed]

Abecassis, J.

D. Muller, C. Wolf, J. Abecassis, R. Millon, A. Engelmann, G. Bronner, N. Rouyer, M. C. Rio, M. Eber, G. Methlin, and P. Basset, “Increased stromelysin 3 gene expression is associated with increased local invasiveness in head and neck squamous cell carcinomas,” Cancer Res. 53(1), 165–169 (1993).
[PubMed]

M. Polette, C. Clavel, D. Muller, J. Abecassis, I. Binninger, and P. Birembaut, “Detection of mRNAs encoding collagenase I and stromelysin 2 in carcinomas of the head and neck by in situ hybridization,” Invasion Metastasis 11(2), 76–83 (1991).
[PubMed]

Akens, M. K.

T. W. Liu, M. K. Akens, J. Chen, L. Wise-Milestone, B. C. Wilson, and G. Zheng, “Imaging of specific activation of photodynamic molecular beacons in breast cancer vertebral metastases,” Bioconjug. Chem. 22(6), 1021–1030 (2011).
[Crossref] [PubMed]

Akram, S.

W. Jerjes, T. Upile, Z. Hamdoon, C. A. Mosse, S. Akram, and C. Hopper, “Photodynamic therapy outcome for oral dysplasia,” Lasers Surg. Med. 43(3), 192–199 (2011).
[Crossref] [PubMed]

Albanese, A.

A. Scerrati, G. M. Della Pepa, G. Conforti, G. Sabatino, A. Puca, A. Albanese, G. Maira, E. Marchese, and G. Esposito, “Indocyanine green video-angiography in neurosurgery: A glance beyond vascular applications,” Clin. Neurol. Neurosurg. 124, 106–113 (2014).
[Crossref] [PubMed]

Ali, N. S.

M. Junaid, M. M. Choudhary, Z. A. Sobani, G. Murtaza, S. Qadeer, N. S. Ali, M. J. Khan, and A. Suhail, “A comparative analysis of toluidine blue with frozen section in oral squamous cell carcinoma,” World J. Surg. Oncol. 10(1), 57 (2012).
[Crossref] [PubMed]

Alizadeh-Naderi, R.

E. Svistun, R. Alizadeh-Naderi, A. El-Naggar, R. Jacob, A. Gillenwater, and R. Richards-Kortum, “Vision enhancement system for detection of oral cavity neoplasia based on auto fluorescence,” Head Neck 26(3), 205–215 (2004).
[Crossref] [PubMed]

Arbogast, S.

C. S. Betz, H. Stepp, P. Janda, S. Arbogast, G. Grevers, R. Baumgartner, and A. Leunig, “A comparative study of normal inspection, autofluorescence and 5-ALA-induced PPIX fluorescence for oral cancer diagnosis,” Int. J. Cancer 97(2), 245–252 (2002).
[Crossref] [PubMed]

A. Leunig, C. S. Betz, M. Mehlmann, H. Stepp, S. Arbogast, G. Grevers, and R. Baumgartner, “Detection of squamous cell carcinoma of the oral cavity by imaging 5-aminolevulinic acid-induced protoporphyrin IX fluorescence,” Laryngoscope 110(1), 78–83 (2000).
[Crossref] [PubMed]

Austin, D. F.

W. J. Blot, J. K. McLaughlin, D. M. Winn, D. F. Austin, R. S. Greenberg, S. Preston-Martin, L. Bernstein, J. B. Schoenberg, A. Stemhagen, and J. F. Fraumeni., “Smoking and drinking in relation to oral and pharyngeal cancer,” Cancer Res. 48(11), 3282–3287 (1988).
[PubMed]

Bao, G.

P. J. Santangelo, B. Nix, A. Tsourkas, and G. Bao, “Dual FRET molecular beacons for mRNA detection in living cells,” Nucleic Acids Res. 32(6), e57 (2004).
[Crossref] [PubMed]

Basset, P.

D. Muller, C. Wolf, J. Abecassis, R. Millon, A. Engelmann, G. Bronner, N. Rouyer, M. C. Rio, M. Eber, G. Methlin, and P. Basset, “Increased stromelysin 3 gene expression is associated with increased local invasiveness in head and neck squamous cell carcinomas,” Cancer Res. 53(1), 165–169 (1993).
[PubMed]

Baumgartner, R.

C. S. Betz, H. Stepp, P. Janda, S. Arbogast, G. Grevers, R. Baumgartner, and A. Leunig, “A comparative study of normal inspection, autofluorescence and 5-ALA-induced PPIX fluorescence for oral cancer diagnosis,” Int. J. Cancer 97(2), 245–252 (2002).
[Crossref] [PubMed]

A. Leunig, C. S. Betz, M. Mehlmann, H. Stepp, S. Arbogast, G. Grevers, and R. Baumgartner, “Detection of squamous cell carcinoma of the oral cavity by imaging 5-aminolevulinic acid-induced protoporphyrin IX fluorescence,” Laryngoscope 110(1), 78–83 (2000).
[Crossref] [PubMed]

Bawendi, M. G.

M. J. Whitley, D. M. Cardona, A. L. Lazarides, I. Spasojevic, J. M. Ferrer, J. Cahill, C.-L. Lee, M. Snuderl, D. G. Blazer, E. S. Hwang, R. A. Greenup, P. J. Mosca, J. K. Mito, K. C. Cuneo, N. A. Larrier, E. K. O’Reilly, R. F. Riedel, W. C. Eward, D. B. Strasfeld, D. Fukumura, R. K. Jain, W. D. Lee, L. G. Griffith, M. G. Bawendi, D. G. Kirsch, and B. E. Brigman, “A mouse-human phase 1 co-clinical trial of a protease-activated fluorescent probe for imaging cancer,” Sci. Transl. Med. 8(320), 320ra4 (2016).
[Crossref] [PubMed]

Bernstein, L.

W. J. Blot, J. K. McLaughlin, D. M. Winn, D. F. Austin, R. S. Greenberg, S. Preston-Martin, L. Bernstein, J. B. Schoenberg, A. Stemhagen, and J. F. Fraumeni., “Smoking and drinking in relation to oral and pharyngeal cancer,” Cancer Res. 48(11), 3282–3287 (1988).
[PubMed]

Betz, C. S.

C. S. Betz, H. Stepp, P. Janda, S. Arbogast, G. Grevers, R. Baumgartner, and A. Leunig, “A comparative study of normal inspection, autofluorescence and 5-ALA-induced PPIX fluorescence for oral cancer diagnosis,” Int. J. Cancer 97(2), 245–252 (2002).
[Crossref] [PubMed]

A. Leunig, C. S. Betz, M. Mehlmann, H. Stepp, S. Arbogast, G. Grevers, and R. Baumgartner, “Detection of squamous cell carcinoma of the oral cavity by imaging 5-aminolevulinic acid-induced protoporphyrin IX fluorescence,” Laryngoscope 110(1), 78–83 (2000).
[Crossref] [PubMed]

Binninger, I.

M. Polette, C. Clavel, D. Muller, J. Abecassis, I. Binninger, and P. Birembaut, “Detection of mRNAs encoding collagenase I and stromelysin 2 in carcinomas of the head and neck by in situ hybridization,” Invasion Metastasis 11(2), 76–83 (1991).
[PubMed]

Birembaut, P.

M. Polette, C. Clavel, D. Muller, J. Abecassis, I. Binninger, and P. Birembaut, “Detection of mRNAs encoding collagenase I and stromelysin 2 in carcinomas of the head and neck by in situ hybridization,” Invasion Metastasis 11(2), 76–83 (1991).
[PubMed]

Bise, K.

W. Stummer, A. Novotny, H. Stepp, C. Goetz, K. Bise, and H. J. Reulen, “Fluorescence-guided resection of glioblastoma multiforme by using 5-aminolevulinic acid-induced porphyrins: a prospective study in 52 consecutive patients,” J. Neurosurg. 93(6), 1003–1013 (2000).
[Crossref] [PubMed]

Bjerring, P.

J. de Leeuw, N. van der Beek, W. D. Neugebauer, P. Bjerring, and H. A. Neumann, “Fluorescence detection and diagnosis of non-melanoma skin cancer at an early stage,” Lasers Surg. Med. 41(2), 96–103 (2009).
[Crossref] [PubMed]

Blazer, D. G.

M. J. Whitley, D. M. Cardona, A. L. Lazarides, I. Spasojevic, J. M. Ferrer, J. Cahill, C.-L. Lee, M. Snuderl, D. G. Blazer, E. S. Hwang, R. A. Greenup, P. J. Mosca, J. K. Mito, K. C. Cuneo, N. A. Larrier, E. K. O’Reilly, R. F. Riedel, W. C. Eward, D. B. Strasfeld, D. Fukumura, R. K. Jain, W. D. Lee, L. G. Griffith, M. G. Bawendi, D. G. Kirsch, and B. E. Brigman, “A mouse-human phase 1 co-clinical trial of a protease-activated fluorescent probe for imaging cancer,” Sci. Transl. Med. 8(320), 320ra4 (2016).
[Crossref] [PubMed]

Blot, W. J.

W. J. Blot, J. K. McLaughlin, D. M. Winn, D. F. Austin, R. S. Greenberg, S. Preston-Martin, L. Bernstein, J. B. Schoenberg, A. Stemhagen, and J. F. Fraumeni., “Smoking and drinking in relation to oral and pharyngeal cancer,” Cancer Res. 48(11), 3282–3287 (1988).
[PubMed]

Bogaards, A.

V. Jayaprakash, M. Sullivan, M. Merzianu, N. R. Rigual, T. R. Loree, S. R. Popat, K. B. Moysich, S. Ramananda, T. Johnson, J. R. Marshall, A. D. Hutson, T. S. Mang, B. C. Wilson, S. R. Gill, J. Frustino, A. Bogaards, and M. E. Reid, “Autofluorescence-guided surveillance for oral cancer,” Cancer Prev. Res. (Phila.) 2(11), 966–974 (2009).
[Crossref] [PubMed]

E. H. Moriyama, A. Kim, A. Bogaards, L. Lilge, and B. C. Wilson, “A Ratiometric Fluorescence Imaging System for Surgical Guidance,” Adv. Opt. Technol. 2008, 1–10 (2008).
[Crossref]

Bogdanov, A.

R. Weissleder, C.-H. Tung, U. Mahmood, and A. Bogdanov., “In vivo imaging of tumors with protease-activated near-infrared fluorescent probes,” Nat. Biotechnol. 17(4), 375–378 (1999).
[Crossref] [PubMed]

Bouquot, J. E.

P. M. Speight, P. M. Farthing, and J. E. Bouquot, “The pathology of oral cancer and precancer,” Curr. Diagn. Pathol. 3(3), 165–176 (1996).
[Crossref]

Bown, S. G.

K. F. M. Fan, C. Hopper, P. M. Speight, G. Buonaccorsi, A. J. MacRobert, and S. G. Bown, “Photodynamic therapy using 5-aminolevulinic acid for premalignant and malignant lesions of the oral cavity,” Cancer 78(7), 1374–1383 (1996).
[Crossref] [PubMed]

W. E. Grant, C. Hopper, A. J. MacRobert, P. M. Speight, and S. G. Bown, “Photodynamic therapy of oral cancer: photosensitisation with systemic aminolaevulinic acid,” Lancet 342(8864), 147–148 (1993).
[Crossref] [PubMed]

Bradford, C. R.

J. C. Brenner, M. P. Graham, B. Kumar, L. M. Saunders, R. Kupfer, R. H. Lyons, C. R. Bradford, and T. E. Carey, “Genotyping of 73 UM-SCC head and neck squamous cell carcinoma cell lines,” Head Neck 32(4), 417–426 (2010).
[PubMed]

Brenner, J. C.

J. C. Brenner, M. P. Graham, B. Kumar, L. M. Saunders, R. Kupfer, R. H. Lyons, C. R. Bradford, and T. E. Carey, “Genotyping of 73 UM-SCC head and neck squamous cell carcinoma cell lines,” Head Neck 32(4), 417–426 (2010).
[PubMed]

Brigman, B. E.

M. J. Whitley, D. M. Cardona, A. L. Lazarides, I. Spasojevic, J. M. Ferrer, J. Cahill, C.-L. Lee, M. Snuderl, D. G. Blazer, E. S. Hwang, R. A. Greenup, P. J. Mosca, J. K. Mito, K. C. Cuneo, N. A. Larrier, E. K. O’Reilly, R. F. Riedel, W. C. Eward, D. B. Strasfeld, D. Fukumura, R. K. Jain, W. D. Lee, L. G. Griffith, M. G. Bawendi, D. G. Kirsch, and B. E. Brigman, “A mouse-human phase 1 co-clinical trial of a protease-activated fluorescent probe for imaging cancer,” Sci. Transl. Med. 8(320), 320ra4 (2016).
[Crossref] [PubMed]

Bronner, G.

D. Muller, C. Wolf, J. Abecassis, R. Millon, A. Engelmann, G. Bronner, N. Rouyer, M. C. Rio, M. Eber, G. Methlin, and P. Basset, “Increased stromelysin 3 gene expression is associated with increased local invasiveness in head and neck squamous cell carcinomas,” Cancer Res. 53(1), 165–169 (1993).
[PubMed]

Buonaccorsi, G.

K. F. M. Fan, C. Hopper, P. M. Speight, G. Buonaccorsi, A. J. MacRobert, and S. G. Bown, “Photodynamic therapy using 5-aminolevulinic acid for premalignant and malignant lesions of the oral cavity,” Cancer 78(7), 1374–1383 (1996).
[Crossref] [PubMed]

Burgess, L.

T. W. Liu, J. Chen, L. Burgess, B. C. Wilson, G. Zheng, L. Zhan, W. K. Liu, and B. Y. Ha, “Activation Kinetics of Zipper Molecular Beacons,” J. Phys. Chem. B 119(1), 44–53 (2015).
[Crossref] [PubMed]

Cahill, J.

M. J. Whitley, D. M. Cardona, A. L. Lazarides, I. Spasojevic, J. M. Ferrer, J. Cahill, C.-L. Lee, M. Snuderl, D. G. Blazer, E. S. Hwang, R. A. Greenup, P. J. Mosca, J. K. Mito, K. C. Cuneo, N. A. Larrier, E. K. O’Reilly, R. F. Riedel, W. C. Eward, D. B. Strasfeld, D. Fukumura, R. K. Jain, W. D. Lee, L. G. Griffith, M. G. Bawendi, D. G. Kirsch, and B. E. Brigman, “A mouse-human phase 1 co-clinical trial of a protease-activated fluorescent probe for imaging cancer,” Sci. Transl. Med. 8(320), 320ra4 (2016).
[Crossref] [PubMed]

Cardona, D. M.

M. J. Whitley, D. M. Cardona, A. L. Lazarides, I. Spasojevic, J. M. Ferrer, J. Cahill, C.-L. Lee, M. Snuderl, D. G. Blazer, E. S. Hwang, R. A. Greenup, P. J. Mosca, J. K. Mito, K. C. Cuneo, N. A. Larrier, E. K. O’Reilly, R. F. Riedel, W. C. Eward, D. B. Strasfeld, D. Fukumura, R. K. Jain, W. D. Lee, L. G. Griffith, M. G. Bawendi, D. G. Kirsch, and B. E. Brigman, “A mouse-human phase 1 co-clinical trial of a protease-activated fluorescent probe for imaging cancer,” Sci. Transl. Med. 8(320), 320ra4 (2016).
[Crossref] [PubMed]

Carey, T. E.

J. C. Brenner, M. P. Graham, B. Kumar, L. M. Saunders, R. Kupfer, R. H. Lyons, C. R. Bradford, and T. E. Carey, “Genotyping of 73 UM-SCC head and neck squamous cell carcinoma cell lines,” Head Neck 32(4), 417–426 (2010).
[PubMed]

Chen, C.-T.

C.-Y. Wang, T. Tsai, C.-P. Chiang, H.-M. Chen, and C.-T. Chen, “Improved diagnosis of oral premalignant lesions in submucous fibrosis patients with 5-aminolevulinic acid induced PpIX fluorescence,” J. Biomed. Opt. 14(4), 044026 (2009).
[Crossref] [PubMed]

Chen, H.-M.

C.-Y. Wang, T. Tsai, C.-P. Chiang, H.-M. Chen, and C.-T. Chen, “Improved diagnosis of oral premalignant lesions in submucous fibrosis patients with 5-aminolevulinic acid induced PpIX fluorescence,” J. Biomed. Opt. 14(4), 044026 (2009).
[Crossref] [PubMed]

Chen, J.

T. W. Liu, J. Chen, L. Burgess, B. C. Wilson, G. Zheng, L. Zhan, W. K. Liu, and B. Y. Ha, “Activation Kinetics of Zipper Molecular Beacons,” J. Phys. Chem. B 119(1), 44–53 (2015).
[Crossref] [PubMed]

T. W. B. Liu, J. Chen, and G. Zheng, “Peptide-based molecular beacons for cancer imaging and therapy,” Amino Acids 41(5), 1123–1134 (2011).
[Crossref] [PubMed]

T. W. Liu, M. K. Akens, J. Chen, L. Wise-Milestone, B. C. Wilson, and G. Zheng, “Imaging of specific activation of photodynamic molecular beacons in breast cancer vertebral metastases,” Bioconjug. Chem. 22(6), 1021–1030 (2011).
[Crossref] [PubMed]

G. Zheng, J. Chen, K. Stefflova, M. Jarvi, H. Li, and B. C. Wilson, “Photodynamic molecular beacon as an activatable photosensitizer based on protease-controlled singlet oxygen quenching and activation,” Proc. Natl. Acad. Sci. U.S.A. 104(21), 8989–8994 (2007).
[Crossref] [PubMed]

Chen, Z. G.

X. Wang, L. Yang, Z. G. Chen, and D. M. Shin, “Application of nanotechnology in cancer therapy and imaging,” CA Cancer J. Clin. 58(2), 97–110 (2008).
[Crossref] [PubMed]

Chiang, C.-P.

C.-Y. Wang, T. Tsai, C.-P. Chiang, H.-M. Chen, and C.-T. Chen, “Improved diagnosis of oral premalignant lesions in submucous fibrosis patients with 5-aminolevulinic acid induced PpIX fluorescence,” J. Biomed. Opt. 14(4), 044026 (2009).
[Crossref] [PubMed]

Choudhary, M. M.

M. Junaid, M. M. Choudhary, Z. A. Sobani, G. Murtaza, S. Qadeer, N. S. Ali, M. J. Khan, and A. Suhail, “A comparative analysis of toluidine blue with frozen section in oral squamous cell carcinoma,” World J. Surg. Oncol. 10(1), 57 (2012).
[Crossref] [PubMed]

Clavel, C.

M. Polette, C. Clavel, D. Muller, J. Abecassis, I. Binninger, and P. Birembaut, “Detection of mRNAs encoding collagenase I and stromelysin 2 in carcinomas of the head and neck by in situ hybridization,” Invasion Metastasis 11(2), 76–83 (1991).
[PubMed]

Coldman, A.

S. Lam, T. Kennedy, M. Unger, Y. E. Miller, D. Gelmont, V. Rusch, B. Gipe, D. Howard, J. C. LeRiche, A. Coldman, and A. F. Gazdar, “Localization of bronchial intraepithelial neoplastic lesions by fluorescence bronchoscopy,” Chest 113(3), 696–702 (1998).
[Crossref] [PubMed]

Conforti, G.

A. Scerrati, G. M. Della Pepa, G. Conforti, G. Sabatino, A. Puca, A. Albanese, G. Maira, E. Marchese, and G. Esposito, “Indocyanine green video-angiography in neurosurgery: A glance beyond vascular applications,” Clin. Neurol. Neurosurg. 124, 106–113 (2014).
[Crossref] [PubMed]

Cuneo, K. C.

M. J. Whitley, D. M. Cardona, A. L. Lazarides, I. Spasojevic, J. M. Ferrer, J. Cahill, C.-L. Lee, M. Snuderl, D. G. Blazer, E. S. Hwang, R. A. Greenup, P. J. Mosca, J. K. Mito, K. C. Cuneo, N. A. Larrier, E. K. O’Reilly, R. F. Riedel, W. C. Eward, D. B. Strasfeld, D. Fukumura, R. K. Jain, W. D. Lee, L. G. Griffith, M. G. Bawendi, D. G. Kirsch, and B. E. Brigman, “A mouse-human phase 1 co-clinical trial of a protease-activated fluorescent probe for imaging cancer,” Sci. Transl. Med. 8(320), 320ra4 (2016).
[Crossref] [PubMed]

de Leeuw, J.

J. de Leeuw, N. van der Beek, W. D. Neugebauer, P. Bjerring, and H. A. Neumann, “Fluorescence detection and diagnosis of non-melanoma skin cancer at an early stage,” Lasers Surg. Med. 41(2), 96–103 (2009).
[Crossref] [PubMed]

De Veld, D. C. G.

D. C. G. De Veld, M. J. H. Witjes, H. J. C. M. Sterenborg, and J. L. N. Roodenburg, “The status of in vivo autofluorescence spectroscopy and imaging for oral oncology,” Oral Oncol. 41(2), 117–131 (2005).
[Crossref] [PubMed]

Della Pepa, G. M.

A. Scerrati, G. M. Della Pepa, G. Conforti, G. Sabatino, A. Puca, A. Albanese, G. Maira, E. Marchese, and G. Esposito, “Indocyanine green video-angiography in neurosurgery: A glance beyond vascular applications,” Clin. Neurol. Neurosurg. 124, 106–113 (2014).
[Crossref] [PubMed]

Derman, A.

M. Scheer, J. Neugebauer, A. Derman, J. Fuss, U. Drebber, and J. E. Zoeller, “Autofluorescence imaging of potentially malignant mucosa lesions,” Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod. 111(5), 568–577 (2011).
[Crossref] [PubMed]

Drake, T. J.

W. Tan, K. Wang, and T. J. Drake, “Molecular beacons,” Curr. Opin. Chem. Biol. 8(5), 547–553 (2004).
[Crossref] [PubMed]

Drebber, U.

M. Scheer, J. Neugebauer, A. Derman, J. Fuss, U. Drebber, and J. E. Zoeller, “Autofluorescence imaging of potentially malignant mucosa lesions,” Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod. 111(5), 568–577 (2011).
[Crossref] [PubMed]

Eber, M.

D. Muller, C. Wolf, J. Abecassis, R. Millon, A. Engelmann, G. Bronner, N. Rouyer, M. C. Rio, M. Eber, G. Methlin, and P. Basset, “Increased stromelysin 3 gene expression is associated with increased local invasiveness in head and neck squamous cell carcinomas,” Cancer Res. 53(1), 165–169 (1993).
[PubMed]

Eckardt, A. M.

M. Rana, A. Zapf, M. Kuehle, N. C. Gellrich, and A. M. Eckardt, “Clinical evaluation of an autofluorescence diagnostic device for oral cancer detection: a prospective randomized diagnostic study,” Eur. J. Cancer Prev. 21(5), 460–466 (2012).
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El-Naggar, A.

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E. H. Moriyama, A. Kim, A. Bogaards, L. Lilge, and B. C. Wilson, “A Ratiometric Fluorescence Imaging System for Surgical Guidance,” Adv. Opt. Technol. 2008, 1–10 (2008).
[Crossref]

G. Zheng, J. Chen, K. Stefflova, M. Jarvi, H. Li, and B. C. Wilson, “Photodynamic molecular beacon as an activatable photosensitizer based on protease-controlled singlet oxygen quenching and activation,” Proc. Natl. Acad. Sci. U.S.A. 104(21), 8989–8994 (2007).
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T. Mang, J. Kost, M. Sullivan, and B. C. Wilson, “Autofluorescence and Photofrin-induced fluorescence imaging and spectroscopy in an animal model of oral cancer,” Photodiagn. Photodyn. Ther. 3(3), 168–176 (2006).
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Figures (5)

Fig. 1
Fig. 1 Molecular beacons comprising a fluorophore (F) conjugated to a quencher (Q) by a short disease-specific linker. In normal tissue the linker remains intact and no fluorescence is observed, while in diseased tissue the linker is specifically cleaved, activating the beacon and enabling fluorescence detection.
Fig. 2
Fig. 2 Representative example from the mouse xenograft model using interstitial administration of PPMMPB or (control) PPMMP, demonstrating tumor-associated fluorescence and whole tongue fluorescence, respectively. A) tongue injected with PPMMPB: i) color white light image pre-injection, ii) monochrome white light image pre-injection, iii) monochrome white light image15 min post injection, iv) fluorescence image pre-injection, v) fluorescence image 15 min post injection showing fluorescence localized to the tumor at the tip of the tongue. B) corresponding images using PPMMP, with the 15 min post injection image (v) showing fluorescence throughout tongue in both healthy and tumor tissue. C) representative H&E stained (i) and confocal fluorescence (ii) of tongue at 15 min post injection of PPMMPB (red: beacon, blue: DAPI). D) corresponding images with PPMMP. E) corresponding images for tongue injected with negative control (DMSO and Tween-80 solution). N = 3 for each group.
Fig. 3
Fig. 3 Representative example of a hamster cheek treated with topical PPMMPB. A) images following 90-95% resection before PPMMPB application: i) color white light, ii) monochrome white light, iii) fluorescence image showing some background fluorescence that is too weak to accurately identify lesions. B) following 15 min topical application of PPMMPB: i) color white light, ii) monochrome white light, iii) fluorescence image showing that the resected area and remnant tumor can be easily visualized. C) representative microscopy images: i) en-face image of H&E stained tissue, and ii) corresponding confocal fluorescence image showing activated PPMMPB at the outer layer of tumor tissue but absent in healthy tissue (red: beacon, blue: DAPI). N = 5 for each group. Note that, for spatial reference, hamster bottom teeth are 1.5cm in length.
Fig. 4
Fig. 4 Representative images of different control hamster cheeks. A) PPMMP-treated, B) negative control-treated (DMSO and Tween-80 solution), C) healthy cheek following surgery and treated with PPMMPB: i) pre-beacon color white light, ii) pre-beacon monochrome white light, iii) pre-beacon fluorescence, iv) post-beacon color white light, v) post-beacon monochrome white light, vi) post-beacon fluorescence. Both healthy and cancerous tissue are fluorescent post-PPMMP application (A,vi). There is no visible fluorescence associated with either the negative control treatment (B,vi) or with PPMMPB applied to surgically-treated healthy tissue (C,vi). D) representative H&E (i) and confocal fluorescence images (ii) in tissue treated with PPMMP, showing non-specific fluorescence in healthy and cancerous tissue with limited penetration. E) corresponding images in tissue with negative control showing fluorescence. F) healthy cheek post-resection and treated with PPMMPB shows no beacon activation. N = 5 for each group. Note that, for spatial reference, hamster bottom teeth are1.5cm in length.
Fig. 5
Fig. 5 Representative HPLC traces A) from beacon extracted from tumor showing intact PPMMPB and PPMMP fragment, B) beacon applied to the tumor, where only intact PPMMPB is present, confirming PPMMPB specificity, not outside of it .C) images before PPMMPB incubation: i) color white light, ii) monochrome white light, iii) fluorescence image showing some background fluorescence, likely caused by bacteria. D) corresponding images after 15 min topical application of PPMMPB: the fluorescence images show that all tumors became fluorescent to different extent as indicated in (E). N = 3 in all cases.

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